Olfactory connectivity mediates sleep-dependent food choices in humans

  1. Surabhi Bhutani
  2. James D Howard
  3. Rachel Reynolds
  4. Phyllis C Zee
  5. Jay Gottfried
  6. Thorsten Kahnt  Is a corresponding author
  1. Northwestern University, United States
  2. San Diego State University, United States
  3. University of Pennsylvania, United States
5 figures and 3 additional files

Figures

Figure 1 with 4 supplements
Experimental design and behavioral effects of sleep deprivation.

(A) Study protocol for deprived sleep (DS) and non-deprived sleep (NDS) sessions with a 19 day washout period. Dinner was served at 6 pm, the fMRI session started at 7 pm, and the ad libitum buffet …

https://doi.org/10.7554/eLife.49053.003
Figure 1—figure supplement 1
Actigraphy data.

(A) Heat maps show individually scored ActiGraph activity data for each subject (rows) in successive time bins (columns) spanning the 7 day sleep stabilization phase and the 1 day sleep …

https://doi.org/10.7554/eLife.49053.004
Figure 1—figure supplement 1—source data 1

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Figure 1—figure supplement 2
No effects of sleep deprivation on anxiety and hormones.

(A) State Anxiety Inventory scores did not differ between DS and NDS sessions (DS: 46.16 ± 0.834, NDS: 44.56 ± 0.951; T24=−1.49, p=0.148). (B) Percent changes in levels of appetite-regulating and …

https://doi.org/10.7554/eLife.49053.005
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Figure 1—figure supplement 3
Odor pleasantness and intensity ratings, and respiratory responses during fMRI.

(A) No sleep-dependent differences in rated odor pleasantness were observed (sleep-by-odor ANOVA; main effect sleep, F1,24=0.54, p=0.470; main effect odor, F2,48=17.08, p=2.50×10−6; sleep-by-odor …

https://doi.org/10.7554/eLife.49053.006
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Figure 1—figure supplement 4
Individual data points for sleep quality, sleepiness, and energy-dense food choices.

(A) Self-report ratings of sleep quality (left) alertness (middle), and well-restedness (right) collected in the morning after the night of sleep manipulation in the NDS and DS session. (B) Stanford …

https://doi.org/10.7554/eLife.49053.007
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Figure 2 with 1 supplement
Sleep-dependent changes in the ECS correlate with energy-dense food choices.

(A) Relative changes in 2-AG and 2-OG levels in the SD condition (% change from NDS baseline). Data are presented as mean ± SEM. (B) Percent changes in 2-OG in DS from NDS baseline correlate …

https://doi.org/10.7554/eLife.49053.030
Figure 2—figure supplement 1
Individual data points for 2-AG and 2-OG.

(A) Serum levels of 2-AG and (B) 2-OG collected during fMRI scanning in the NDS and DS session. Circles represent individual data points and diagonal represents identity line.

https://doi.org/10.7554/eLife.49053.031
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Figure 3 with 2 supplements
Sleep deprivation enhances encoding of odor information in piriform cortex.

(A) Sweet and savory food odors and non-food control odors presented during fMRI. (B) Schematic of the searchlight decoding analysis used to reveal information about food vs. non-food odors in the …

https://doi.org/10.7554/eLife.49053.036
Figure 3—figure supplement 1
Decoding of odor information across sleep sessions.

(A) Coronal and (B) axial sections showing significant decoding accuracy for food vs non-food odors (averaged across sleep sessions) in piriform cortex (x = 16, y=−2, z=−14, T24 = 4.20, PFWE-SVC = 0.…

https://doi.org/10.7554/eLife.49053.037
Figure 3—figure supplement 2
fMRI signal coverage.

(A) Coronal and (B) axial sections of a normalized EPI scans averaged across subjects and sessions. Numbers indicate y- and z-coordinates in MNI space, respectively.

https://doi.org/10.7554/eLife.49053.038
Sleep deprivation does not enhance univariate fMRI responses to odors.

(A) Significant univariate odor-evoked fMRI responses (food and non-food odors > clean air) in piriform cortex, averaged across both sleep sessions (right, x = 22, y = −4, z = −18, T24 = 12.53, PFWE …

https://doi.org/10.7554/eLife.49053.039
Piriform-insula connectivity mediates the effects of 2-OG on sleep-dependent food choices.

(A) Sleep-dependent changes in odor-evoked connectivity (odor >clean air) between piriform cortex and insula negatively correlated with the energy density of foods consumed at the post-fMRI buffet …

https://doi.org/10.7554/eLife.49053.041

Additional files

Supplementary file 1

Sleep monitoring (actigraphy) data.

Means ± SEM of time in bed (TIB), total sleep time (TST), wake after sleep onset (WASO), and sleep efficiency (SE) in the DS and NDS session for the week of sleep stabilization (average across seven nights) and the night of sleep manipulation. P-values from paired t-tests of the difference between NDS and DS sessions.

https://doi.org/10.7554/eLife.49053.044
Supplementary file 2

Ratings of odor stimuli during screening session.

Means ± SEM of ratings for pleasantness, intensity, quality (sweet vs savory), and edibility for the six food and two non-food odors used in this study. For each subject, four food and two non-food odors were presented. Numbers in parenthesis indicate the number of subjects for which a given odor was selected. F- and P-values from one-way ANOVAs across odors.

https://doi.org/10.7554/eLife.49053.045
Transparent reporting form
https://doi.org/10.7554/eLife.49053.046

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